Nutrient fluxes, oxygen consumption and fatty acid composition from deep-water demo- and hexactinellid sponges from New Zealand

Abstract

Sponges are an important component of deep-water ecosystems enhancing eukaryotic biodiversity by hosting diverse endo- and epibiota and providing three dimensional habitats for benthic invertebrates and fishes. As holobionts they are important hosts of microorganisms which are involved in carbon and nitrogen cycling. While increasing exploration of deep-water habitats results in new sponge species being discovered, little is known about their physiology and role in nutrient fluxes. Around New Zealand (Southwest Pacific), the sponge biodiversity is particularly high, and we selected six deep-sea sponge clusters (Saccocalyx, Suberites, Tedania, Halichondria/ Dendoricella, Sceptrulophora, Lissodendoryx) for in-situ and ex-situ experiments. We investigated the biochemical composition of the sponges, measured oxygen consumption and inorganic nutrient fluxes, as well as bacterial and phospholipid-derived fatty acid (PLFA) compositions. Our aim was to assess differences in fluxes and fatty acid composition among sponge clusters and linking their bacterial communities to nitrogen cycling processes. All sponges excreted nitrite and ammonia. Nitrate and phosphate excretion were independent of phylum affiliation (Demospongiae, Hexactinellida). Nitrate was excreted by the Halichondria/ Dendoricella and Lissodendoryx clusters, whereas the Suberites, Tedania, and Sceptrulophora clusters consumed it. Phosphate was excreted by Sceptrulophora and Halichondria/ Dendoricella clusters and consumed by all other clusters. Silicon was consumed by all sponge clusters, except for Saccocalyx and Halichondria/ Dendoricella clusters. Oxygen consumption rates ranged from 0.17 to 3.56+-0.60 mmol O2 g C d-1. The PLFA composition was very sponge-cluster dependent and consisted mostly of long-chain fatty acids. Most PLFAs were sponge-specific, followed by bacteria-specific PLFAs, and others. All sponge clusters, except for Suberites, were low-microbial abundance (LMA) sponges whose bacterial community composition was dominated by Proteobacteria, Bacteroidota, Planctomycetota, and Nitrospinota. The Suberites cluster consisted of high-microbial abundance (HMA) sponges with Proteobacteria, Chloroflexota, Acidobacteriota, and Actinobacteriota as dominant bacteria. Based on the inorganic nitrogen flux measurements, we identified three types of nitrogen cycling in the sponges: In type 1, sponges (Dendoricella spp. indet., Lissodendoryx cluster) respired aerobically and ammonificated organic matter (OM) to ammonium, fixed N2 to ammonium, and nitrified aerobically heterotrophically produced ammonium to nitrate and nitrite. In type 2, sponges (Halichondria sp., Sceptrulophora, Suberites, Tedania clusters) respired OM aerobically and ammonificated it to ammonium. They also reduced nitrate anaerobically to ammonium via dissimilatory nitrate reduction to ammonium. In type 3, ammonium was microbially nitrified to nitrite and afterwards to nitrate presumably by ammonium-oxidizing Bacteria and/ or Archaea.

Dissolved organic matter fluxes and fatty acid composition from shallow-water and deep-water demo- and hexactinellid sponges from New Zealand

“…Species-specific conversion factors are presented in Table S2. PLFAs from freeze-dried sponge tissue were extracted following a modified protocol of the Bligh and Dyer extraction method (Bligh and Dyer, 1959; de Kluijver, 2021; de Kluijver et al, 2021) as described in (Stratmann et al, 2024). The bacterial community composition of sponges was extracted and analyzed as described in (Stratmann et al, 2024).…”

“…C, % DM)/ δ 13 org. C content of the sponges were determined as described in detail in (Stratmann et al, 2024). Species-specific conversion factors are presented in Table S2.…”

“…consisted of only three different PLFAs (Table S7). The class of Hexactinellida sponges is characterized by a reduced diversity of PLFAs (Stratmann et al, 2024;Thiel et al, 2002a), very long C chains of 28 to 32 C atoms, and a lack of C chains with 24 to 28 C atoms (Thiel et al, 2002a) Bennett et al, (2018), sponges may adapt to increasing water temperatures by increasing the mean chain length of their fatty acids and increasing the degree of unsaturation of fatty acids when they are phototrophic sponges or decreasing the degree of unsaturation of fatty acids when they are heterotrophic sponges. These adaptations could not be found in Tedania sp.…”

“…A comparison of the PLFA composition of F. raoulensis with the composition of two specimens of the Sceptrulophora cluster fromStratmann et al, (2024) showed a very close resemblance in the relative abundance of the individual PLFAs, but F. raoulensis' PLFA composition deviated from the PLFA composition of Saccocalyx tetractinus(Reiswig and Kelly, 2018). The latter contained almost 40% C29:2ω?, but <10% C30:3ω?(Stratmann et al, 2024), whereas F. raoulensis had <10% C29:2ω? and about 25% C30:3ω?.…”

“…from Raoul Island (6 m water depth; this paper) lived at an ambient temperature of 25°C, while Tedania sp. from Pegasus canyon, off Canterbury (852 m depth;(Stratmann et al, 2024)) lived at 6°C. Following observations by…”